Anatomical and functional examination of superior colliculus projections to the inferior olivary neurons in mice

The Inferior olive (IO) is an important region for motor learning and movement coordination. Its climbing fibers projection to the Purkinje neurons in the cerebellar cortex is a sole source of the complex spikes, characterized by a strong depolarization in the Purkinje neuron’s dendrites. To generate spikes, the IO relies on inputs from various regions of the brain, including the superior colliculus (SC), a midbrain structure known for its role in orienting behaviors.

This study investigates SC projections to the IO using viral tracers, calcium imaging, and optogenetic stimulation. We reveal that, in addition to the known projections to the medial accessory olive (MAO), SC axons also project to the ventral principal olive (PO). Despite projecting to different parts of the IO, SC-MAO and SC-PO neurons are intermingled within the lateral part of the SC with similar gross morphology. We show that SC axons terminate on both dendritic shafts and spines of IO neurons, potentially influencing not only spiking probability, but also the network synchronization mediated by gap junctions coupling on the dendritic spines.

As a proof of principle, we recorded the in-vivo activity of neurons in ventral PO using calcium indicators and show that optogenetic activation of SC inputs can evoke spiking and enhance synchronization in IO neurons.